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Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex

“Sense of agency” (SoA), the feeling of control for events caused by one's own actions, is deceived by visuomotor incongruence. Sensorimotor networks are implicated in SoA, however little evidence exists on brain functionality during agency processing. Concurrently, it has been suggested that t...

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Autores principales: Piras, Federica, Vecchio, Daniela, Ciullo, Valentina, Gili, Tommaso, Banaj, Nerisa, Piras, Fabrizio, Spalletta, Gianfranco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7469779/
https://www.ncbi.nlm.nih.gov/pubmed/32667099
http://dx.doi.org/10.1002/hbm.25107
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author Piras, Federica
Vecchio, Daniela
Ciullo, Valentina
Gili, Tommaso
Banaj, Nerisa
Piras, Fabrizio
Spalletta, Gianfranco
author_facet Piras, Federica
Vecchio, Daniela
Ciullo, Valentina
Gili, Tommaso
Banaj, Nerisa
Piras, Fabrizio
Spalletta, Gianfranco
author_sort Piras, Federica
collection PubMed
description “Sense of agency” (SoA), the feeling of control for events caused by one's own actions, is deceived by visuomotor incongruence. Sensorimotor networks are implicated in SoA, however little evidence exists on brain functionality during agency processing. Concurrently, it has been suggested that the brain's intrinsic resting‐state (rs) activity has a preliminary influence on processing of agency cues. Here, we investigated the relation between performance in an agency attribution task and functional interactions among brain regions as derived by network analysis of rs functional magnetic resonance imaging. The action‐effect delay was adaptively increased (range 90–1,620 ms) and behavioral measures correlated to indices of cognitive processes and appraised self‐concepts. They were then regressed on local metrics of rs brain functional connectivity as to isolate the core areas enabling self‐agency. Across subjects, the time window for self‐agency was 90–625 ms, while the action‐effect integration was impacted by self‐evaluated personality traits. Neurally, the brain intrinsic organization sustaining consistency in self‐agency attribution was characterized by high connectiveness in the secondary visual cortex, and regional segregation in the primary somatosensory area. Decreased connectiveness in the secondary visual area, regional segregation in the superior parietal lobule, and information control within a primary visual cortex‐frontal eye fields network sustained self‐agency over long‐delayed effects. We thus demonstrate that self‐agency is grounded on the intrinsic mode of brain function designed to organize information for visuomotor integration. Our observation is relevant for current models of psychopathology in clinical conditions in which both rs activity and sense of agency are altered.
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spelling pubmed-74697792020-09-09 Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex Piras, Federica Vecchio, Daniela Ciullo, Valentina Gili, Tommaso Banaj, Nerisa Piras, Fabrizio Spalletta, Gianfranco Hum Brain Mapp Research Articles “Sense of agency” (SoA), the feeling of control for events caused by one's own actions, is deceived by visuomotor incongruence. Sensorimotor networks are implicated in SoA, however little evidence exists on brain functionality during agency processing. Concurrently, it has been suggested that the brain's intrinsic resting‐state (rs) activity has a preliminary influence on processing of agency cues. Here, we investigated the relation between performance in an agency attribution task and functional interactions among brain regions as derived by network analysis of rs functional magnetic resonance imaging. The action‐effect delay was adaptively increased (range 90–1,620 ms) and behavioral measures correlated to indices of cognitive processes and appraised self‐concepts. They were then regressed on local metrics of rs brain functional connectivity as to isolate the core areas enabling self‐agency. Across subjects, the time window for self‐agency was 90–625 ms, while the action‐effect integration was impacted by self‐evaluated personality traits. Neurally, the brain intrinsic organization sustaining consistency in self‐agency attribution was characterized by high connectiveness in the secondary visual cortex, and regional segregation in the primary somatosensory area. Decreased connectiveness in the secondary visual area, regional segregation in the superior parietal lobule, and information control within a primary visual cortex‐frontal eye fields network sustained self‐agency over long‐delayed effects. We thus demonstrate that self‐agency is grounded on the intrinsic mode of brain function designed to organize information for visuomotor integration. Our observation is relevant for current models of psychopathology in clinical conditions in which both rs activity and sense of agency are altered. John Wiley & Sons, Inc. 2020-07-15 /pmc/articles/PMC7469779/ /pubmed/32667099 http://dx.doi.org/10.1002/hbm.25107 Text en © 2020 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Piras, Federica
Vecchio, Daniela
Ciullo, Valentina
Gili, Tommaso
Banaj, Nerisa
Piras, Fabrizio
Spalletta, Gianfranco
Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex
title Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex
title_full Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex
title_fullStr Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex
title_full_unstemmed Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex
title_short Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex
title_sort sense of external agency is sustained by multisensory functional integration in the somatosensory cortex
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7469779/
https://www.ncbi.nlm.nih.gov/pubmed/32667099
http://dx.doi.org/10.1002/hbm.25107
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